Feeding rate and attack specialization: the roles of predator experience and energetic tradeoffs

Synopsis Individual mosquitofish, Gambusia affinis, can adopt a broad range of attack selectivities. In part, this variation can be explained by the past experiences of a fish. Individuals selected the more profitable Ceriodaphnia dubia (Cladocera) over less profitable cyclopoid copepods to a greater degree after being exposed to both prey types than did individuals experienced with only one of the prey types. Feeding rate (biomass ingested per unit time) declined with increased attack specialization on the profitable prey (Ceriodaphnia) when such prey were scarce, a result in agreement with assumptions of optimal diet theory. When profitable prey were abundant feeding rate was a bimodal function of the intensity of specialization on profitable prey; fish that specialized on cyclopoid copepods (the less profitable prey type) fed at higher rates than did generalists. This may be the result of antagonistic learning that precluded feeding efficiently on more than one type of prey at a time. The data are consistent with the hypothesis that rejection of unsuitable prey involves a time cost. The two preceeding aspects of foraging behavior, which are absent from most optimal diet models, could lead to failure in predicting the attack specialization of some predators, An additional aspect of the results was the generally weak relationship between feeding efficiency and specialization behavior. This suggests that feeding rate may not have been as tightly linked to the specialization behavior a predator adopts as is assumed by current foraging theory.     

Prey choice by marten during a decline in prey abundance

Summary We examined variation in diet choice by marten (Martes americana) among seasons and between sexes and ages from 1980–1985. During this period prey populations crashed simultaneously, except for ruffed grouse (Bonasa umbellus) which was common at the beginning and end of the study, and masked shrews (Sorex cinereus) which were abundant in 1983. Marten were catholic in selection of prey and made use of most available mammalian prey, ruffed grouse, passerine birds, berries, and insects. Diet niche was widest during the latter three years when prey was scare, particularly in late winter. Diet niche breadth was negatively correlated with abundance of all common prey species. Proportion of small prey species in the diet was correlated with absolute abundance of those species, but proportion of some large prey was related to their relative abundance. Diet choice varied among years and among seasons. Berries and insects were common in summer diets while large prey, particularly varying hare (Lepus americanus), were more frequent in winter diet than in summer diet. We found little evidence that any small mammal species was a preferred prey. Sexual size dimorphism between the sexes did not affect prey choice, nor did age. Reduced foraging effort in winter resulted in a wider diet niche only when prey was scarce. The only prediction of optimal foraging models fully supported by our data was a wider diet niche with reduced prey abundance. However, among the three most profitable prey species choice was dependent on the absolute abundance of the most profitable type (varying hare). We suggest that marten primarily forage for large prey but employ a strategy which results in encounters with small prey as well. These small prey are eaten as they provide energy at minimal cost, between captures of large prey.     

Prey abundance vs diet breadth in a spider test system

Summary Decisions made as to what prey types to include in the diet were analysed for two populations of the spider,Agelenopsis aperta existing under markedly different prey availability and predation levels. Potential prey types were ranked as to their relative profitabilities with respect to energy gain per handling effort and predation risk. Members of the population experiencing limited prey availability but low risk of predation to visually hunting predators exhibited a significantly higher capture attempt rate towards all prey encountered than the population for which prey were abundant but for which predation was a significant problem. Neither spider population preferentially attacked prey that exhibited higher profitability rankings. An experiment was completed that indicates thatA. aperta can discriminate between more and less profitable prey. Suggestions are made as to why the population experiencing abundant food did not exhibit a narrower diet when compared to the population existing under limited food.     

Laboratory and field studies on diet choice in three-spined sticklebacks, Gasterosteus aculeatus L., in relation to profitability and visual features of prey

Diet choice by three-spined sticklebacks was investigated under both laboratory and field conditions. In the laboratory, sticklebacks did not always choose the more profitable of two prey items; instead, they apparently selected prey according to a set of proximate decision rules based on visual cues provided by the prey. Studies of the diet of sticklebacks in the field suggest that they may use the same set of proximate decision rules to select their food and that in these more complex conditions this may lead them to feed preferentially on the more profitable types of prey. In general, sticklebacks selected zooplanktonic rather than benthic prey (which is less profitable), but the importance of benthos in the diet increased as the density of zooplankton decreased.     

Feeding Experience Modifies the Assessment of Ambush Sites by the Timber Rattlesnake, a Sit-and-Wait Predator

To effectively ambush prey, sit‐and‐wait predators must locate sites where profitable prey are likely to return. One means by which predators evaluate potential ambush sites is by recognizing high‐use areas through chemical cues deposited inadvertently by their prey. However, it is unknown whether ambush predators can use chemical cues associated with past prey items in the assessment of potential ambush sites. I examined selection of ambush sites by timber rattlesnakes (Crotalus horridus) exposed to trails made from chemical extracts of the integument of various prey species. I evaluated the role of feeding experience in ambush site selection by comparing the behavior of timber rattlesnakes before and after feeding experience with different sized prey items. Timber rattlesnakes are more likely to select ambush sites adjacent to chemical trails from prey with which they have had feeding experience, but only those fed relatively large prey showed an increase in responsiveness. Increased responsiveness after feeding experience was exhibited in experiments using integumentary extracts of mammals (the natural prey of timber rattlesnakes), but not in those using extracts of fish. These results indicate that ambush predators may learn to recognize chemicals on the integument of profitable food items, and use that experience when subsequently selecting ambush sites. Additionally, these findings provide evidence that size‐dependent predation by snakes may be, in some species, a result of active prey selection.     

Variation in the effect of profitability on prey size selection by the lacertid lizard Psammodromus algirus

Maximizing the average rate of energy intake (profitability) may not always be the optimal foraging strategy for ectotherms with relatively low energy requirements. To test this hypothesis, we studied the feeding behaviour of captive insectivorous lizards Psammodromus algirus, and we obtained experimental estimates of prey mass, handling time, profitability, and attack distance for several types of prey. Handling time increased linearly with prey mass and differed significantly among prey types when prey size differences were controlled for, and mean profitabilities differed among prey taxa, but profitability was independent of prey size. The attack distance increased with prey length and with the mobility of prey, but it was unrelated to profitability. Thus, lizards did not seem to take account of the rate of energy intake per second as a proximate cue eliciting predatory behavior. This information was combined with pitfall-trap censuses of prey (in late April, mid-June and late July) that allowed us to compare the mass of the prey captured in the environment with that of the arthropods found in the stomachs of sacrificed free-living lizards. In April, when food abundance was low and lizards were reproducing, profitability had a pronounced effect on size selection and lizards selected prey larger than average from all taxa except the least profitable ones. As the active season progressed, and with a higher availability of food, the number of prey per stomach decreased and their mean ize increased. The effect of profitability on size selection decreased (June) and eventually vanished (July–August). This variation is probably related to seasonal changes in the ecology of lizards, e.g. time minimization in the breeding season as a means of saving time for nonforaging activities versus movement minimization by selecting fewer (but larger) prey in the postbreeding season. Thus, the hypothesis that maximizing profitability could be just an optional strategy for a terrestrial ectothermic vertebrate was supported by our data.     

The evolution of locomotory behavior in profitable and unprofitable simulated prey

Prey that are unprofitable to attack (for example, those containing noxious chemicals) frequently exhibit slower and more predicable movement than species that lack these defenses. Possible explanations for the phenomenon include a lack of selection pressure on unprofitable prey to avoid predators and active selection on unprofitable prey to advertise their noxiousness. We explicitly tested these and other hypotheses using a novel artificial world in which the locomotory characteristics (step size, waiting time, and angular direction) of artificial profitable and unprofitable computer-generated prey were subject to continued selection by humans over a number of generations. Unprofitable prey evolved significantly slower movement behavior than profitable prey when they were readily recognized as unprofitable, and also when they frequently survived predatory attacks. This difference arose primarily as a consequence of more intense selection on profitable prey to avoid capture. When unprofitable prey were very similar (but not identical) in morphological appearance to profitable prey, unprofitable prey evolved particularly slow movement behavior, presumably because when they were slow-moving they could be more readily recognized as being unprofitable. When unprofitable prey were constrained to move slowly, a morphologically identical profitable prey species evolved locomotor mimicry only when it had no more effective means of avoiding predation. Overall, our results provide some of the first empirical support for a number of earlier hypotheses for differences in movement between unprofitable and profitable prey and demonstrate that locomotor mimicry is not an inevitable outcome of selection even in morphologically similar prey.     

Prey selection by plovers: Optimal foraging in mixed-species groups

Prey (earthworm) size selection was investigated in lapwings (Vanellus vanellus) and golden plovers (Pluvialis apricaria) feeding in mixed species flocks and compared with that predicted by an optimal foraging model based on energy intake. As well as the usual constraints of searching and handling time, our model incorporated the difficulty of capturing concealed prey, the orientation time needed to locate prey and the risk of theft by gulls (Larus ridibundus). When costs were taken into account, small worms turned out to be the most profitable. The relative profitability of size classes changed when gulls were present and birds shifted their intake accordingly so that they always took mainly the most profitable worms. Birds were expected to do best by taking the three most profitable size classes and the size range taken was consistent with this. In addition there was an inverse relationship between the probabilities of taking profitable and unprofitable worm sizes. Observations of birds were supported by field enclosure experiments which prevented birds feeding in certain areas. Departures from predictions of the model are interpreted as sampling errors due to birds using depth as an approximate indicator of worm size.     

Oviposition strategy of the parasitic waspDinarmus basalis (Hymenoptera,Pteromalidae)

Summary Host type choice and sex allocation were examined using the solitary parasitic waspDinarmus basalis (Pteromalidae, Hymenoptera) parasitizing larvae or pupae of the bean weevilCallosobruchus chinensis (Bruchidae, Coleoptera) within azuki beans (Vigna angularis). The wasps were offered two types of host; one was hard for the mother to lay eggs in, but was more beneficial for the offspring; the other was easy for the mother to lay eggs in, but was less beneficial for the offspring. The two types of host were one large host (17-day old host) in one bean and 6 small hosts (12-, or 13-day old hosts) in one bean. The same number of each host was presented at the same time to female wasps. The wasps accepted more 17-day old hosts than 12-day old hosts, and more 13-day old hosts than 17-day old hosts in each pair-wise choice experiment. The proportions of accepted host types were different from the proportions predicted by optimization models of random prey encounter with known or unknown prey densities. The wasps showed partial preference of host types. Incomplete information about prey densities, and about the costs and benefits of the two types of host may have generated the partial preference. Two predictions of host sizemodels, that (1) there should be a negative relationship between host size and offspring sex ratio (proportion of male offsprings), and (2) the sex ratio in each size host changes with the relative frequency of each size host utilized, were qualitatively supported.     

Foraging Decision Rules and Prey Species Preferences of Northwestern Crows (Corvus caurinus)

Categorization of similar prey types and the application of decision rules by dietary generalists can enhance the efficiency of foraging decisions and facilitate the inclusion of novel prey types in the diet. While considerable research attention has been directed toward investigation of these concepts in invertebrates, few have assessed categorization and decision rules used by generalist vertebrate predators. In this study, we experimentally investigated decision rules and prey preferences of northwestern crows (Corvus caurinus) feeding on littleneck clams (Tapes philippinarum) and whelks (Nucella lamellosa). We presented crows with three species‐size combinations: small clams (2.0–2.9 cm length) paired with large whelks (4.0–4.9 cm), small clams paired with medium whelks (3.0–3.9 cm), and large clams (4.0–4.9 cm) with large whelks. Profitability estimates based on observations of crows feeding on these prey species indicated that clams were always the more energetically profitable option; however, in prey choice trials crows consistently selected the heavier prey species, regardless of differences in profitability. These results show that crows apply a general decision rule according to which they select heavier prey items when feeding on hard‐shelled prey requiring similar handling techniques, and that while such decision rules may approximate optimal choices they may not always follow predictions based solely on prey profitability. We discuss these results in the context of behavioural flexibility of generalist predators, and predicting impacts of intertidal avian predators on prey populations.     

Learning affects prey selection in larvae of a generalist coccinellid predator

Under natural conditions, generalist predatory insects have to cope with a variety of potential prey species that are not all equally suitable. Under these circumstances, learning may be adaptive if it allows adjustment to variations in resource quality and availability. Under laboratory conditions, we examined the learning ability and memory in the prey selection process of larvae of the predatory coccinellid Coleomegilla maculata ssp. lengi Timberlake (Coleoptera: Coccinellidae). Using choice tests, we studied prey rejection behaviour of C. maculata fourth instars towards prey of different quality and we also tested the influence of hunger and prior experience with other food types on the prey rejection behaviour of coccinellid larvae. Coleomegilla maculata larvae gradually changed their behaviour and rejected low‐quality hosts more frequently, whereas high‐quality hosts were nearly always accepted. After 48 h, the learned behaviour appeared to be partially forgotten. Hunger and experience with other food types prior to the test had little effect on the gradual change of behaviour but the quality of the food ingested influenced the initial level of prey rejection. Our results demonstrate that (1) C. maculata larvae can adjust their prey selection behaviour with experience to reject progressively less suitable prey, and (2) previous experience with other prey types can influence their initial preference.     

Optimal foraging on the roof of the world: Himalayan langurs and the classical prey model

Optimal foraging theory has only been sporadically applied to nonhuman primates. The classical prey model, modified for patch choice, predicts a sliding “profitability threshold” for dropping patch types from the diet, preference for profitable foods, dietary niche breadth reduction as encounter rates increase, and that exploitation of a patch type is unrelated to its own abundance. We present results from a 1‐year study testing these predictions with Himalayan langurs (Semnopithecus entellus) at Langtang National Park, Nepal. Behavioral data included continuous recording of feeding bouts and between‐patch travel times. Encounter rates were estimated for 55 food types, which were analyzed for crude protein, lipid, free simple sugar, and fibers. Patch types were entered into the prey model algorithm for eight seasonal time periods and differing age‐sex classes and nutritional currencies. Although the model consistently underestimated diet breadth, the majority of nonpredicted patch types represented rare foods. Profitability was positively related to annual/seasonal dietary contribution by organic matter estimates, whereas time estimates provided weaker relationships. Patch types utilized did not decrease with increasing encounter rates involving profitable foods, although low‐ranking foods available year‐round were taken predominantly when high‐ranking foods were scarce. High‐ranking foods were taken in close relation to encounter rates, while low‐ranking foods were not. The utilization of an energetic currency generally resulted in closest conformation to model predictions, and it performed best when assumptions were most closely approximated. These results suggest that even simple models from foraging theory can provide a useful framework for the study of primate feeding behavior. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Food selectivity versus prey availability: a study using the marine fish Pomatoschistus microps

Summary The food selection of the common goby, Pomatoschistus microps Krøyer, was studied in the field and in laboratory experiments on the Swedish west coast. The three most important prey organisms for P. microps in the study area were Corophium volutator, chironomid larvae and Nereis spp. Corophium was consumed more than any other prey, even when it was not the most abundant prey species in the bottom. One reason may be the higher activity of Corophium above the sediment surface, which may increase its visibility and consequently its vulnerability to visual predators. When P. microps was offered Corophium and chironomid larvae with similar exposure in laboratory experiments, it showed no preference for either of the prey items. It always took the closest mobile prey, regardless of species and size.     

Individual variation in prey choice in a predator-prey community

One predator-two prey community models are studied with an emphasis on individual variation in predator behavior. The predator behaves according to a well-known prey choice model. The behavioral model predicts that predators should always attack the primary prey (more profitable prey of the two), but only attack the alternative prey (less profitable prey of the two) when the density of the primary prey is below a threshold density. The predator that accepts the alternative prey does not discriminate between the primary and alternative prey (all-or-nothing preference for the alternative prey). However, empirical studies do not result in clear all-or-nothing responses. Previous models examined the relaxation of the all-or-nothing response by assuming partial preference (e.g., predators preferentially forage on the primary prey even when they also attack the alternative prey). In this study, I consider individual variation in two predator traits (prey density perception and handling time) as the sources of the variation in the threshold density, which can make empirical data appear deviated from the expectation. I examine how community models with partial preference and individual variation differ in their dynamics and show that the differences can be substantial. For example, the dynamics of a model based on individual variation can be more stable (e.g., stable in a wider parameter region) than that of a model based on partial preference. As the general statistical property (Jensen’s inequality) is a main factor that causes the differences, the results of the study have general implications to the interpretation of models based on average per-capita rates.     

Wait Until Dark? Daily Activity Patterns and Nest Predation by Snakes

Predation involves costs and benefits, so predators should employ tactics that reduce their risk of injury or death and that increase their success at capturing prey. One potential way that predators could decrease risk and increase benefits is by attacking prey at night when risks may be reduced and prey more vulnerable. Because some snakes are facultatively nocturnal and prey on bird nests during the day and night, they are ideal for assessing the costs and benefits of diurnal vs. nocturnal predation. We used automated radiotelemetry and cameras to investigate predation on nesting birds by two species of snakes, one diurnal and the other facultatively nocturnal. We predicted that snakes preying on nests at night should experience less parental nest defence and capture more adults and nestlings. Rat snakes (Pantherophis obsoletus) were relatively inactive at night (23–36% activity) but nearly always preyed on nests after dark (80% of nest predations). Conversely, racers (Coluber constrictor) were exclusively diurnal and preyed on nests during the times of day they were most active. These results are consistent with rat snakes strategically using their capacity for facultative nocturnal activity to prey on nests at night. The likely benefit is reduced nest defence because birds defended their nests less vigourously at night. Consistent with nocturnal predation being safer, rat snake predation events lasted three times longer at night than during the day (26 vs. 8 min). Nocturnal nest predation did not make nests more profitable by increasing the likelihood of capturing adults or removing premature fledging of nestlings. The disconnect between rat snake activity and timing of nest predation seems most consistent with rat snakes locating prey during the day using visual cues but waiting until dark to prey on nests when predation is safer, although designing a direct test of this hypothesis will be challenging.     

Sublethal costs associated with the consumption of toxic prey by snakes

Costs of plant defences to herbivores have been extensively studied, but costs of chemical defences to carnivores are less well understood. We examine the costs to Australian keelback snakes (Tropidonophis mairii, Gray 1841) of consuming cane toads (Bufo[Rhinella]marinus Linnaeus 1758). Cane toads (an invasive species in Australia) are highly toxic. Although keelbacks can consume toads without dying (unlike most Australian snakes), we show that cane toads are poor quality prey for keelbacks. Toads are of low net nutritional value, take longer to consume than do native frogs and reduce the snake's locomotor performance for up to 6 h after ingestion of a meal. These latter effects may increase a snake's vulnerability to predation. Nutritional content of vertebrate prey is not the only factor driving the evolution of foraging behaviour; other more subtle costs, such as risk of predation, may be widespread.     

The influence of predation risk on diet selectivity: A theoretical analysis

Studies that have examined the effect of experimental increases in predation risk on diet selectivity have shown both decreased and increased diet selectivity. A possible explanation for these disparate results emerges from an examination of the prey sets used in these studies, which differed in the relationship between the values of risk components associated with the capture of different prey types (‘danger’) and their profitabilities. When less profitable prey were more dangerous, selectivity increased with predation risk. When prey were equally dangerous, selectivity did not change. Finally, when the more profitable prey were also more dangerous, selectivity decreased with risk. Here, we examine theoretically the influence of a forager's estimate of the probability that a predator is present (φ) on the selection of diets from prey sets with varying danger–profitability relationships. A dynamic programming model is used to determine the maximum attack time (or distance) for each of two types of prey, differing in their energetic content, for a range of forager energy state and φ levels. The diets which would result if foragers attacked prey according to the rules provided by the dynamic model are then determined. The model results indicate that the prey danger–profitability relationship determines the diet selectivity response to φ, confirming that variation in this relationship could be responsible for the range of experimental results. This revised version was published online in July 2006 with corrections to the Cover Date.     

Pikeperch Sander lucioperca trapped between niches: foraging performance and prey selection in a piscivore on a planktivore diet

The foraging behaviour of planktivorous pikeperch Sander lucioperca during their first growing season was analysed. Field data showed that S. lucioperca feed on extremely rare prey at the end of the summer, suggesting the presence of a bottleneck. In experiments, foraging ability of planktivorous S. lucioperca was determined when fish were feeding on different prey types (Daphnia magna or Chaoborus spp.) and sizes (D. magna of lengths 1 or 2·5 mm) when they occurred alone. From these results, the minimum density requirement of each prey type was analysed. The energy gain for three different foraging strategies was estimated; a specialized diet based on either large D. magna or Chaoborus spp. or a generalist diet combining both prey types. Prey value estimates showed that Chaoborus spp. should be the preferred prey, assuming an energy maximizing principle. In prey choice experiments, S. lucioperca largely followed this principle, including D. magna in the diet only when the density of the Chaoborus spp. was below a threshold value. Splitting the foraging bout into different sequences, however, resulted in a somewhat different pattern. During an initial phase, S. lucioperca captured both prey as encountered and then switched to Chaoborus spp. if prey density was above the threshold level. The prey selection observed was mainly explained by sampling behaviour and incomplete information about environmental quality, whereas satiation only had marginal effects. It was concluded that the observed diet based on rare prey items was in accordance with an optimal foraging strategy and may generate positive growth in the absence of prey fish in suitable sizes.     

Prey size selection and cannibalistic behaviour of juvenile barramundi Lates calcarifer

This study assessed the cannibalistic behaviour of juvenile barramundi Lates calcarifer and examined the relationship between prey size selection and energy gain of cannibals. Prey handling time and capture success by cannibals were used to estimate the ratio of energy gain to energy cost in prey selection. Cannibals selected smaller prey despite its capability of ingesting larger prey individuals. In behavioural analysis, prey handling time significantly increased with prey size, but it was not significantly affected by cannibal size. Conversely, capture success significantly decreased with the increase of both prey and cannibal sizes. The profitability indices showed that the smaller prey provides the most energy return for cannibals of all size classes. These results indicate that L. calcarifer cannibals select smaller prey for more profitable return. The behavioural analysis, however, indicates that L. calcarifer cannibals attack prey of all size at a similar rate but ingest smaller prey more often, suggesting that prey size selection is passively orientated rather than at the predator's choice. The increase of prey escape ability and morphological constraint contribute to the reduction of intracohort cannibalism as fish grow larger. This study contributes to the understanding of intracohort cannibalism and development of strategies to reduce fish cannibalistic mortalities.     

Natural selection on unpalatable species imposed by state-dependent foraging behaviour

Müllerian mimicry is typically thought to arise as a consequence of defended prey species adopting a similar way of signalling their unprofitability, thereby reducing the costs of predator education. Here we consider subsequent selection on the morphology of prey species, in the potentially lengthy period of time when predators are generally aware of the noxious qualities of their prey (and so no further learning is involved). Using a pair of stochastic dynamic programming equations which describe both the toxin burdens of a predator and its energy level, we identified the optimal state-dependent rules that maximize a predator's long-term survivorship, and examined the implications of this behaviour for the evolution of prey morphologies. When palatable prey are in short supply then those prey species which contain relatively low doses of toxins become profitable to consume by hungry predators. Under these conditions, a weakly defended prey could gain selective advantage in the post educational period by resembling a prey species which contained a higher dose of the same or different toxins, although the precise nature of the ecological relationship between model and mimic could either be mutualistic or parasitic depending on how mimic density increases when favoured by selection. Our work formally demonstrates that one does not always need to invoke educational effects to explain why two or more unpalatable species have evolved a similar appearance, or to explain why mimetic similarity among distasteful species is maintained over time. When two species contain high levels of different toxins then they may gain mutual advantage by resembling one another, not only by educating the predator as to their common unprofitability (classical Müllerian mimicry), but also by increasing predator uncertainty as to the specific kind of toxin a prey item contains.